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Prevalence and diversity of Hepatozoon canis in naturally infected dogs in Japanese islands and peninsulas

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Abstract

Canine hepatozoonosis is a worldwide protozoal disease caused by Hepatozoon canis and Hepatozoon americanum and is transmitted by ixodid ticks, Rhipicephalus and Amblyomma spp., respectively. H. canis infection is widespread in Africa, Europe, South America, and Asia, including Japan. The objective of this study was to study the distribution pattern and diversity of H. canis in naturally infected dogs in nine Japanese islands and peninsulas. Therefore, 196 hunting dogs were randomly sampled during the period from March to September 2011 and the ages and sexes were identified. Direct microscopy using Giemsa-stained blood smears revealed H. canis gametocytes in the peripheral blood of 45 (23.6 %) dogs. Polymerase chain reaction (PCR) was performed on EDTA-anticoagulated blood, initially with the common primer set (B18S-F and B18S-R) amplifying the 1,665-bp portion of the 18S rRNA gene, and then with the specific primer set (HepF and HepR) amplifying about 660 bp fragments of the same gene. Based on PCR, 84 (42.9 %) dogs were positive using the common primer and 81 (41.3 %) were positive using the specific primer. The current investigation indicated that all screened areas, except for Sado Island and Atsumi Peninsula, were infected. Yaku Island had the highest infection rate (84.6 % in males and 100.0 % in females), while Ishigaki Island showed the lowest infection rates (8.3 % in males and 17.7 % in females). Both sexes were infected with no significant difference. However, diversity of infection among the surveyed islands and peninsulas was significantly different (P < 0.05). Although H. canis has previously been reported in dogs in Japan, the higher infection rate described in the current study and the diversity of infection in a wide range of islands strongly encourage prospective studies dealing with the prevention and treatment of the infection in dogs, as well as control of ticks.

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References

  • Aktas M, Özübek S, Say n Ipek DN (2013) Molecular investigations of Hepatozoon species in dogs and developmental stages of Rhipicephalus sanguineus. Parasitol Res 112:2381–2385

    Article  PubMed  Google Scholar 

  • Amoli AAR, Khoshnegah J, Razmi Gh R (2012) A preliminary parasitological survey of Hepatozoon spp. infection in dogs in Mashhad, Iran. Iranian J Parasitol 7(4):99–103

    Google Scholar 

  • Assarasakorn S, Niwetpathomwat A, Techangamsuwan S, Suvarnavibhaja S (2006) A retrospective study of clinical hematology and biochemistry of canine hepatozoonosis on hospital populations in Bangkok, Thailand. Comp Clin Pathol 15:107–109

    Article  Google Scholar 

  • Baneth G, Harmelin A, Presentey BZ (1995) Hepatozoon canis infection in two dogs. J Am Vet Med Assoc 206:1891–1894

    PubMed  CAS  Google Scholar 

  • Baneth G, Shkap V, Presentey B, Pipano E (1996) Hepatozoon canis: the prevalence of antibodies and gametocytes in dogs in Israel. Vet Res Commun 20:41–46

    Article  PubMed  CAS  Google Scholar 

  • Baneth G, Weigler B (1997) Retrospective case–control study of hepatozoonosis in dogs in Israel. J Vet Intern Med 11:365–370

    Article  PubMed  CAS  Google Scholar 

  • Baneth G, Barta JR, Shkap V, Martin DS, Macintire DK, Vincent-Johnson N (2000) Genetic and antigenic evidence supports the separation of Hepatozoon canis and Hepatozoon americanum at the species level. J Clin Microbiol 38:1298–1301

    PubMed  CAS  Google Scholar 

  • Baneth G, Samish M, Alekseev E, Aroch I, Shkap V (2001) Transmission of Hepatozoon canis to dogs by naturally-fed or percutaneously-injected Rhipicephalus sanguineus ticks. J Parasitol 87(3):606–611

    PubMed  CAS  Google Scholar 

  • Baneth G, Mathew JS, Shkap V, Macintire DK, Barta JR, Ewing SA (2003) Canine hepatozoonosis: two disease syndromes caused by separate Hepatozoon spp. Trends Parasitol 19:27–31

    Article  PubMed  Google Scholar 

  • Cummings CA, Panciera RJ, Kocan KM, Mathew JS, Ewing SA (2005) Characterization of stages of Hepatozoon americanum and of parasitized canine host cells. Vet Pathol 42:788–796

    Article  PubMed  CAS  Google Scholar 

  • Dantas-Torres F (2008) The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Vet Parasitol 152:173–185

    Article  PubMed  Google Scholar 

  • Elias E, Homans PA (1988) Hepatozoon canis infection in dogs: clinical and hematological findings; treatment. J Small Anim Pract 29:55–62

    Article  Google Scholar 

  • Ezekolli CD, Ogunkoya AB, Abdullahi R, Tekedec LB, Sannusi A, Ilemobade AA (1983) Clinical and epidemiological studies on canine hepatozoonosis in Zaria, Nigeria. J Small Anim Pract 24:455–460

    Article  Google Scholar 

  • Fischer S, Hartmann K, Gothe R (1994) Hepatozoon canis: an important parasitic infection in dogs. Tierarztl Prax 22:172–180

    PubMed  CAS  Google Scholar 

  • Forlano M, Scofield A, Elisei C, Fernandes KR, Ewing SA, Massard CL (2005) Diagnosis of Hepatozoon spp. in Amblyomma ovale and its experimental transmission in domestic dogs in Brazil. Vet Parasitol 134:1–7

    Article  PubMed  CAS  Google Scholar 

  • Forlano MD, Teixeira KRS, Scofield A, Elisei C, Yotoko KSC, Fernandes KR, Linhares GFC, Ewing SA, Massard CL (2007) Molecular characterization of Hepatozoon sp. from Brazilian dogs and its phylogenetic relationship with other Hepatozoon spp. Vet Parasitol 145:21–30

    Article  PubMed  CAS  Google Scholar 

  • Garcia de Sá A, Cerqueira AF, O’Dwyer LH, Abreu F, Ferreira RF, Pereira AM, Velho PB, Rubini AS, Almosny NRP (2007) Detection of Hepatozoon spp. in naturally infected Brazilian dogs by polymerase chain reaction. Intern J Appl Res Vet Med 5(2):49–51

    Google Scholar 

  • Gavazza A, Bizzeti M, Papini R (2003) Observations on dogs found naturally infected with Hepatozoon canis in Italy. Rev Med Vet 154:565–571

    Google Scholar 

  • Gondim LFP, Kohayagawa A, Alencar NX, Biondo AW, Takahira RK, Franco SRV (1998) Canine hepatozoonosis in Brazil: description of eight naturally occurring cases. Vet Parasitol 74:319–323

    Article  PubMed  CAS  Google Scholar 

  • Groves MG, Dennis GL, Amyx HL, Hursll DL (1975) Am J Vet Res 36:937–940

    PubMed  CAS  Google Scholar 

  • Hervas J, Carrasco L, Gomez-Villamandos JC (1995) Acute fatal hepatozoonosis in a puppy: histological and ultrastructural study. Vet Rec 137:518–519

    Article  PubMed  CAS  Google Scholar 

  • Holland M (2001) Emerging diseases in northern Europe. J Small Anim Pract 42:205–206

    Article  PubMed  CAS  Google Scholar 

  • Ibrahim NDG, Rahamathulla PM, Njoku CO (1989) Neutrophil myeloperoxidase deficiency associated with canine hepatozoonosis. Int J Parasitol 19(8):915–918

    Article  PubMed  CAS  Google Scholar 

  • Inokuma H, Ohno K, Yamamoto S (1999) Serosurvey of Ehrlichia canis and Hepatozoon canis infection in dogs in Yamaguchi Prefecture, Japan. J Vet Med Sci 61(10):1153–1155

    Article  PubMed  CAS  Google Scholar 

  • Inokuma H, Okuda M, Ohno K, Shimoda K, Onishi T (2002) Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Vet Parasitol 106:265–271

    Article  PubMed  CAS  Google Scholar 

  • Inokuma H, Yoshizaki Y, Shimada Y, Sakata Y, Okuda M, Onishi T (2003) Epidemiological survey of Babesia species in Japan performed with specimens from ticks collected from dogs and detection of new Babesia DNA closely related to Babesia odocoilei. J Clin Microbiol 41:3494–3498

    Article  PubMed  CAS  Google Scholar 

  • Jittapalapong S, Rungphisutthipongse O, Maruyama S, Schaefer JJ, Stich RW (2006) Detection of Hepatozoon canis in stray dogs and cats in Bangkok, Thailand. Ann NY Acad Sci 1081:479–488

    Article  PubMed  CAS  Google Scholar 

  • Karagenc TI, Pasa S, Kirli G, Hosgor M, Bilgic HB, Ozon YH, Atasoy A, Eren H (2006) A parasitological, molecular and serological survey of Hepatozoon canis infection in dogs around the Aegean coast of Turkey. Vet Parasitol 13:113–119

    Article  Google Scholar 

  • Li Y, Wang C, Allen KE, Little SE, Ahluwalia SK, Gao D, Macintire DK, Blagburn BL, Kaltenboeck B (2008) Diagnosis of canine Hepatozoon spp. infection by quantitative PCR. Vet Parasitol 157:50–58

    Article  PubMed  CAS  Google Scholar 

  • Macintire DK, Vincent-Johnson N, Dillon AR, Blagburn B, Lindsay DS, Whitley EM, Banfield C (1997) Canine hepatozoonosis: in dogs of 22 cases (1989–1994). J Am Vet Med Assoc 210:916–922

    PubMed  CAS  Google Scholar 

  • Makimura S, Kinjo H, Matovelo JA, Ogawa H, Yamaguchi R, Matsuyama K, Tateyama S, Yamasaki K, Usui M (1991) Three cases of Hepatozoon canis infection of dogs in Miyazaki Prefecture. J Jpn Vet Med Assoc 44:928–932 (in Japanese with English summary)

    Google Scholar 

  • Mathew JS, Van Den Bussche RA, Ewing AS, Malayer JR, Latha BR, Panciera RJ (2000) Phylogenetic relationships of Hepatozoon (Apicomplexa: Adeleorina) based on molecular, morphologic and life-cycle characters. J Parasitol 86:366–372

    PubMed  CAS  Google Scholar 

  • Mathew JS, Saliki JT, Ewing SA, Lehenbauer TW, Panciera RJ, Malayer JR, Cummings CA, Kocan AA (2001) An indirect enzyme-linked immunosorbent assay for diagnosis of American canine hepatozoonosis. J Vet Diagn Invest 13:17–21

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Shiramizu K, Hara Y, Inoue M, Shimoda K, Nakama S (1991) First case of Hepatozoon canis infection of a dog in Japan. J Vet Med Sci 53:1097–1099

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Inoue M, Tateyama S, Taura Y, Nakama S (1993a) Vertical transmission of Hepatozoon canis in dogs. J Vet Med Sci 55:867–868

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Shimoda K, Inoue M, Shiramizu K, Kanoe M, Taura Y, Nakama S (1993b) Seasonal periodical appearance of Hepatozoon canis gamont in the peripheral blood. J Vet Med Sci 55:877–879

    Article  PubMed  CAS  Google Scholar 

  • Murata T, Amimoto T, Shiramizu K, Hara Y, Inoue M, Kanoe M, Uzuka Y, Taura Y, Nakama S (1993c) Survey of canine Hepatozoon canis infection in the western area of Yamaguchi Prefecture. J Jpn Vet Med Assoc 46:395–397 (in Japanese with english summary)

    Google Scholar 

  • Murata T, Inoue M, Taura Y, Nakama S, Abe H, Fujisaki K (1995) Detection of Hepatozoon canis oocyst from ticks collected from the infected dogs. J Vet Med Sci 57(1):111–112

    Article  PubMed  CAS  Google Scholar 

  • Nayel M, El-Dakhly Kh M, Aboulaila M, Elsify A, Hassan H, Ibrahim E, Salama A, Yanai T (2012) The use of different diagnostic tools for Babesia and Theileria parasites in cattle in Menofia, Egypt. Parasitol Res 111(3):1019–1024

    Article  PubMed  Google Scholar 

  • O’Dwyer LH, Massard CL, de Souza JCP (2001) Hepatozoon canis infection associated with dog ticks of rural areas of Rio de Janeiro State, Brazil. Vet Parasitol 94:143–150

    Article  PubMed  Google Scholar 

  • O’Dwyer LH, Saito ME, Hasegawa MY, Kohayagawa A (2004) Tissue stages of Hepatozoon canis in naturally infected dogs from Sao Paulo State, Brazil. Parasitol Res 94:240–242

    Article  PubMed  Google Scholar 

  • Otranto D, Dantas-Torres F, Weigl S, Latrofa MS, Stanneck D, de Caprariis D, Capelli G, Baneth G (2011) Diagnosis of Hepatozoon canis in young dogs by cytology and PCR. Parasites Vectors 4:55

    Article  PubMed  Google Scholar 

  • Oyamada M, Davoust B, Boni M, Dereure J, Bucheton B, Hammad A, Itamoto K, Okuda M, Inokuma H (2005) Detection of Babesia canis rossi, B. canis vogeli, and Hepatozoon canis in dogs in a village of eastern Sudan by using a screening PCR and sequencing methodologies. Clin Diagn Lab Immunol 12(11):1343–1346

    PubMed  CAS  Google Scholar 

  • Pasa S, Kiral F, Karagenc T, Atasoy A, Seyrek K (2009) Description of dogs naturally infected with Hepatozoon canis in the Aegean region of Turkey. Turk J Vet Anim Sci 33(4):289–295

    CAS  Google Scholar 

  • Perez RR, Rubini AS, O’Dwyer LH (2004) The first report of Hepatozoon spp. (Apicomplexa, Hepatozoidae) in domestic cats from Sao Paulo state, Brazil. Parasitol Res 94:83–85

    Article  PubMed  Google Scholar 

  • Rajamanickam C, Weisenhutter E, Zin FMD, Hamid J (1985) The incidence of canine hematozoa in peninsular Malaysia. Vet Parasitol 17:151–157

    Article  PubMed  CAS  Google Scholar 

  • Rubini AS, Paduan KD, Cavalcante GG, Ribolla PE, O’Dwyer LH (2005) Molecular identification and characterization of canine Hepatozoon species from Brazil. Parasitol Res 97:91–93

    Article  PubMed  Google Scholar 

  • Rubini AS, Paduan KD, Lopes VVA, O’Dwyer LH (2008) Molecular and parasitological survey of Hepatozoon canis (Apicomplexa: Hepatozoidae) in dogs from rural area of Sao Paulo state, Brazil. Parasitol Res 102:895–899

    Article  PubMed  Google Scholar 

  • Rubini AS, Paduan KD, Martins TF, Labruna MB, O’Dwyer LH (2009) Acquisition and transmission of Hepatozoon canis (Apicomplexa: Hepatozoidae) by the tick Amblyomma ovale (Acari: Ixodidae). Vet Parasitol 164:324–327

    Article  PubMed  CAS  Google Scholar 

  • Sasaki M, Omobowale O, Tozuka M, Ohta K, Matsuu A, Nottidge HO, Hirata H, Ikadai H, Oyamada T (2007) Molecular Survey of Babesia canis in dogs in Nigeria. J Vet Med Sci 69(11):1191–1193

    Article  PubMed  CAS  Google Scholar 

  • Sasaki M, Omobowale O, Ohta K, Tozuka M, Matsuu A, Hirata H, Nottidge HO, Ikadai H, Oyamada T (2008) A PCR-based epidemiological survey of Hepatozoon canis in dogs in Nigeria. J Vet Med Sci 70(7):743–745

    Article  PubMed  CAS  Google Scholar 

  • Shaw SE, Day MJ, Birtles RJ, Breitschwerdt EB (2001) Tick-borne infectious diseases of dogs. Trends Parasitol 17:74–80

    Article  PubMed  CAS  Google Scholar 

  • Smith TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). J Parasitol 82:565–585

    Article  PubMed  CAS  Google Scholar 

  • Spolidorio MG, Labruna MB, Zago AM, Donatele DM, Caliari KM, Yoshinari NH (2009) Hepatozoon canis infecting dogs in the State of Espirito Santo, southeastern Brazil. Vet Parasitol 163:357–361

    Article  PubMed  Google Scholar 

  • Tamboura HH, Banga-Mboko H, Maes D, Youssao I, Traore A, Bayala B, Dembele MA (2006) Prevalence of common gastrointestinal nematode parasites in scavenging pigs of different ages and sexes in eastern centre province, Burkina Faso. Onderstepoort J Vet Res 73:53–60

    Article  PubMed  CAS  Google Scholar 

  • Vargas-Hernandez G, André MR, Munhoz TD, Faria JML, Machado RZ, Tinucci-Costa M (2012) Molecular characterization of Hepatozoon canis in dogs from Colombia. Parasitol Res 110:489–492

    Article  PubMed  Google Scholar 

  • Vincent-Johnson NA, Macintire DK, Lindsay DL, Lenz SD, Baneth G, Shkap V, Blagburn BL (1997) A new Hepatozoon species from dogs: description of the causative agent of canine hepatozoonosis in North America. J Parasitol 83:1165–1172

    Article  PubMed  CAS  Google Scholar 

  • Vojta L, Mrljak V, Curković S, Zivicnjak T, Marinculić A, Beck R (2009) Molecular epizootiology of canine hepatozoonosis in Croatia. Int J Parasitol 39:1129–1136

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was partially supported by a Grant-in-Aid for scientific research from the Ministry of Health, Labor and Welfare in Japan and was also supported by a grant from Hokkaido University, Japan.

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Correspondence to Tokuma Yanai.

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El-Dakhly, K.M., Goto, M., Noishiki, K. et al. Prevalence and diversity of Hepatozoon canis in naturally infected dogs in Japanese islands and peninsulas. Parasitol Res 112, 3267–3274 (2013). https://doi.org/10.1007/s00436-013-3505-1

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